Below-ground soil microorganisms can modulate above-ground plant-insect interactions. It still needs to be determined whether this is a direct effect of single species or an indirect effect of shifts in soil microbial community assemblages. Evaluation of the soil microbiome as a whole is critical for understanding multi-trophic interactions, including those mediated by volatiles involving plants, herbivorous insects, predators/parasitoids and microorganisms. We implemented a regulated system comprising Nerium oleander plants grown in soil initially containing a sterile/non sterile inoculum, herbivore Aphis nerii and predator Chrysoperla carnea. After aphid attack, plants emitted a characteristic blend of volatiles derived from two biosynthetic classes: fatty acid catabolites and aromatic-derived products. Three aliphatic compounds were mainly detected in plants grown in the inoculated microbial soil, a blend which was preferentially chosen by C. carnea adult females. The contrasting effect of the initial inocula was attributed to the different microbial consortia developed in each treatment. We argue that differences in the relative abundance of the active microbial communities in the rhizosphere correlate with those in the emission of selected volatile compounds by attacked plants. The mechanisms involved in how the functional soil microbiome modulates inducible indirect defence of plants are discussed.